Allelic Variation and Transcriptional Isoforms of Wheat TaMYC1 Gene Regulating Anthocyanin Synthesis in Pericarp

Recently the TaMYC1 gene encoding bHLH transcription factor has been isolated from the bread wheat (Triticum aestivum L.) genome and shown to co-locate with the Pp3 gene conferring purple pericarp color. As a functional evidence of TaMYC1 and Pp3 being the same, higher transcriptional activity of the TaMYC1 gene in colored pericarp compared to uncolored one has been demonstrated. In the current study, we present additional strong evidences of TaMYC1 to be a synonym of Pp3. Furthermore, we have found differences between dominant and recessive Pp3(TaMyc1) alleles. Light enhancement of TaMYC1 transcription was paralleled with increased AP accumulation only in purple-grain wheat. Coexpression of TaMYC1 and the maize MYB TF gene ZmC1 induced AP accumulation in the coleoptile of white-grain wheat. Suppression of TaMYC1 significantly reduced AP content in purple grains. Two distinct TaMYC1 alleles (TaMYC1p and TaMYC1w) were isolated from purple- and white-grained wheat, respectively. A unique, compound cis-acting regulatory element had six copies in the promoter of TaMYC1p, but was present only once in TaMYC1w. Analysis of recombinant inbred lines showed that TaMYC1p was necessary but not sufficient for AP accumulation in the pericarp tissues. Examination of larger sets of germplasm lines indicated that the evolution of purple pericarp in tetraploid wheat was accompanied by the presence of TaMYC1p. Our findings may promote more systematic basic and applied studies of anthocyanins in common wheat and related Triticeae crops.

[1]  Huicong Wang,et al.  Transcriptome Profiling of Light-Regulated Anthocyanin Biosynthesis in the Pericarp of Litchi , 2016, Front. Plant Sci..

[2]  Dengcai Liu,et al.  Transcriptome Analysis of Purple Pericarps in Common Wheat (Triticum aestivum L.) , 2016, PloS one.

[3]  Stacey D. Smith,et al.  Molecular evolution of anthocyanin pigmentation genes following losses of flower color , 2016, BMC Evolutionary Biology.

[4]  Yong-chen Du,et al.  The Tomato Hoffman’s Anthocyaninless Gene Encodes a bHLH Transcription Factor Involved in Anthocyanin Biosynthesis That Is Developmentally Regulated and Induced by Low Temperatures , 2016, PloS one.

[5]  Baolong Liu,et al.  Identification of a candidate gene for Rc-D1, a locus controlling red coleoptile colour in wheat , 2016 .

[6]  Min Zhang,et al.  Altered Phenylpropanoid Metabolism in the Maize Lc-Expressed Sweet Potato (Ipomoea batatas) Affects Storage Root Development , 2016, Scientific Reports.

[7]  Aizhong Liu,et al.  Light signaling induces anthocyanin biosynthesis via AN3 mediated COP1 expression , 2015, Plant signaling & behavior.

[8]  C. Santos-Buelga,et al.  Anthocyanin and phenolic characterization, chemical composition and antioxidant activity of chagalapoli (Ardisia compressa K.) fruit: A tropical source of natural pigments , 2015 .

[9]  S. Taketa,et al.  Isolation of candidate genes for the barley Ant1 and wheat Rc genes controlling anthocyanin pigmentation in different vegetative tissues , 2015, Molecular Genetics and Genomics.

[10]  E. Khlestkina,et al.  The Regulation of Anthocyanin Synthesis in the Wheat Pericarp , 2014, Molecules.

[11]  Cathie Martin,et al.  Engineering anthocyanin biosynthesis in plants. , 2014, Current opinion in plant biology.

[12]  Wendy Harwood,et al.  Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance , 2013, Journal of experimental botany.

[13]  E. Khlestkina,et al.  Genes determining the coloration of different organs in wheat , 2013, Russian Journal of Genetics: Applied Research.

[14]  A. Börner,et al.  Variability of Rc (red coleoptile) alleles in wheat and wheat-alien genetic stock collections , 2011 .

[15]  Qianhua Shen,et al.  Molecular analysis of common wheat genes encoding three types of cytosolic heat shock protein 90 (Hsp90): functional involvement of cytosolic Hsp90s in the control of wheat seedling growth and disease resistance. , 2011, The New phytologist.

[16]  P. Salimath,et al.  PHENOLIC ACID PROFILES AND ANTIOXIDANT ACTIVITIES OF DIFFERENT WHEAT (TRITICUM AESTIVUM L.) VARIETIES , 2011 .

[17]  M. Maekawa,et al.  Development of PCR markers for Tamyb10 related to R-1, red grain color gene in wheat , 2011, Theoretical and Applied Genetics.

[18]  M. Nair,et al.  Anthocyanin content, antioxidant, anti-inflammatory and anticancer properties of blackberry and raspberry fruits , 2010 .

[19]  J. López‐Bucio,et al.  Plant Immunity Induced by Oligogalacturonides Alters Root Growth in a Process Involving Flavonoid Accumulation in Arabidopsis thaliana , 2010, Journal of Plant Growth Regulation.

[20]  Xuesen Chen,et al.  Anthocyanin biosynthesis in pears is regulated by a R2R3-MYB transcription factor PyMYB10 , 2010, Planta.

[21]  T. Nakamura,et al.  Grain color development and the inheritance of high anthocyanin blue aleurone and purple pericarp in spring wheat (Triticum aestivum L.). , 2009 .

[22]  Sunggil Kim,et al.  Identification of two novel inactive DFR-A alleles responsible for failure to produce anthocyanin and development of a simple PCR-based molecular marker for bulb color selection in onion (Allium cepa L.) , 2009, Theoretical and Applied Genetics.

[23]  G. Stoner,et al.  Anthocyanins and their role in cancer prevention. , 2008, Cancer letters.

[24]  Atul Puri,et al.  Mutations in Phytoene Desaturase Gene in Fluridone-Resistant Hydrilla (Hydrilla verticillata) Biotypes in Florida , 2007, Weed Science.

[25]  Tao Chen,et al.  Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. , 2007, The Plant journal : for cell and molecular biology.

[26]  G. Mazza,et al.  Bioactivity, Absorption, and Metabolism of Anthocyanins , 2007 .

[27]  S. Iida,et al.  A bHLH regulatory gene in the common morning glory, Ipomoea purpurea, controls anthocyanin biosynthesis in flowers, proanthocyanidin and phytomelanin pigmentation in seeds, and seed trichome formation. , 2007, The Plant journal : for cell and molecular biology.

[28]  T. Lacombe,et al.  Wine grape (Vitis vinifera L.) color associates with allelic variation in the domestication gene VvmybA1 , 2007, Theoretical and Applied Genetics.

[29]  A. R. Walker,et al.  Light-Induced Expression of a MYB Gene Regulates Anthocyanin Biosynthesis in Red Apples1 , 2006, Plant Physiology.

[30]  D. Treutter.  Significance of flavonoids in plant resistance: a review , 2006 .

[31]  C. Owens,et al.  265) DNA Sequence Variation within the Promoter of VvmybA1 Associates with Flesh Pigmentation of Intensely Colored Grape Varieties , 2006 .

[32]  H. Qin,et al.  Molecular and functional characterization of sulfiredoxin homologs from higher plants , 2006, Cell Research.

[33]  G. Muday,et al.  Ethylene Modulates Flavonoid Accumulation and Gravitropic Responses in Roots of Arabidopsis1[W] , 2006, Plant Physiology.

[34]  M. Thomson,et al.  Caught Red-Handed: Rc Encodes a Basic Helix-Loop-Helix Protein Conditioning Red Pericarp in Rice[W][OA] , 2006, The Plant Cell Online.

[35]  B. Gill,et al.  Development of a Virus-Induced Gene-Silencing System for Hexaploid Wheat and Its Use in Functional Analysis of the Lr21-Mediated Leaf Rust Resistance Pathway1 , 2005, Plant Physiology.

[36]  Y. Sano,et al.  Allelic Diversification at the C (OsC1) Locus of Wild and Cultivated Rice , 2004, Genetics.

[37]  M. Maekawa,et al.  Transient Expression of Anthocyanin in Developing Wheat Coleoptile by Maize C1 and B-peru Regulatory Genes for Anthocyanin Synthesis , 2003 .

[38]  Andrea Brandolini,et al.  Genetics and geography of wild cereal domestication in the near east , 2002, Nature Reviews Genetics.

[39]  Daowen Wang,et al.  Identification of a novel HMW glutenin subunit and comparison of its amino acid sequence with those of homologous subunits , 2002 .

[40]  Richard A. Dixon,et al.  Activation Tagging Identifies a Conserved MYB Regulator of Phenylpropanoid Biosynthesis , 2000, Plant Cell.

[41]  C. Tonelli,et al.  The developmental expression of the maize regulatory gene Hopi determines germination-dependent anthocyanin accumulation. , 2000, Genetics.

[42]  M. T. Selvi,et al.  Sunlight-induced anthocyanin pigmentation in maize vegetative tissues , 1999 .

[43]  J. Mol,et al.  Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. , 1998, The Plant journal : for cell and molecular biology.

[44]  C. Tonelli,et al.  Light-Dependent Spatial and Temporal Expression of Pigment Regulatory Genes in Developing Maize Seeds. , 1997, The Plant cell.

[45]  T. Holton,et al.  Genetics and Biochemistry of Anthocyanin Biosynthesis. , 1995, The Plant cell.

[46]  R. Solano,et al.  Dual DNA binding specificity of a petal epidermis‐specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. , 1995, The EMBO journal.

[47]  S. Goff,et al.  Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. , 1992, Genes & development.

[48]  A. C. Zeven.  Wheats with purple and blue grains: a review , 1991, Euphytica.

[49]  C. Tonelli,et al.  Genetic and molecular analysis of Sn, a light-inducible, tissue specific regulatory gene in maize , 1991, Molecular and General Genetics MGG.

[50]  S. Wessler,et al.  Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[51]  H. Saedler,et al.  The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto‐oncogene products and with structural similarities to transcriptional activators. , 1987, The EMBO journal.

[52]  C. Qualset,et al.  Bulk populations in wheat breeding: comparison of single-seed descent and random bulk methods , 1975, Euphytica.

[53]  O. Ceska,et al.  DEVELOPMENTAL DIFFERENCES IN ACTION OF R AND B ALLELES IN MAIZE , 1973 .

[54]  B. Mcclintock.  The origin and behavior of mutable loci in maize , 1950, Proceedings of the National Academy of Sciences.

[55]  E. Khlestkina,et al.  Allelic state of the genes conferring purple pigmentation in different wheat organs predetermines transcriptional activity of the anthocyanin biosynthesis structural genes , 2013 .

[56]  K. Saraswathi,et al.  Establishment of enhanced anthocyanin production in Malva sylvestris L. with different induced stress. , 2012 .

[57]  T. Beta,et al.  Effect of thermal processing on antioxidant properties of purple wheat bran , 2007 .

[58]  小林 省藏,et al.  Association of VvmybA1 Gene Expression with Anthocyanin Production in Grape (Vitis vinifera) Skin-color Mutants , 2005 .

[59]  H. Hirochika,et al.  Association of VvmybA1 gene expression with anthocyanin production in grape (Vitis vinifera) skin-color mutants , 2005 .

[60]  E. Coen,et al.  Floral Homoeotic and Pigment Mutations Produced by Transposon-Mutagenesis in Antirrhinum majus , 1991 .